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Open Access Research article

A carboxylesterase, Esterase-6, modulates sensory physiological and behavioral response dynamics to pheromone in Drosophila

Thomas Chertemps1, Adrien François12, Nicolas Durand1, Gloria Rosell3, Teun Dekker4, Philippe Lucas2 and Martine Maïbèche-Coisne1*

Author Affiliations

1 Université Pierre et Marie Curie, UMR 1272, Physiologie de l'Insecte, Signalisation et Communication, F-75252, Paris, France

2 INRA, UMR 1272, Physiologie de l'Insecte, Signalisation et Communication, F-78026, Versailles, France

3 University of Barcelona, Faculty of Pharmacy, Unit of Medicinal Chemistry, 08028, Barcelona, Spain

4 Swedish University of Agricultural Sciences, Department of Plant Protection Biology, 23053, Alnarp, Sweden

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BMC Biology 2012, 10:56  doi:10.1186/1741-7007-10-56

Published: 21 June 2012

Abstract

Background

Insects respond to the spatial and temporal dynamics of a pheromone plume, which implies not only a strong response to 'odor on', but also to 'odor off'. This requires mechanisms geared toward a fast signal termination. Several mechanisms may contribute to signal termination, among which odorant-degrading enzymes. These enzymes putatively play a role in signal dynamics by a rapid inactivation of odorants in the vicinity of the sensory receptors, although direct in vivo experimental evidences are lacking. Here we verified the role of an extracellular carboxylesterase, esterase-6 (Est-6), in the sensory physiological and behavioral dynamics of Drosophila melanogaster response to its pheromone, cis-vaccenyl acetate (cVA). Est-6 was previously linked to post-mating effects in the reproductive system of females. As Est-6 is also known to hydrolyze cVA in vitro and is expressed in the main olfactory organ, the antenna, we tested here its role in olfaction as a putative odorant-degrading enzyme.

Results

We first confirm that Est-6 is highly expressed in olfactory sensilla, including cVA-sensitive sensilla, and we show that expression is likely associated with non-neuronal cells. Our electrophysiological approaches show that the dynamics of olfactory receptor neuron (ORN) responses is strongly influenced by Est-6, as in Est-6° null mutants (lacking the Est-6 gene) cVA-sensitive ORN showed increased firing rate and prolonged activity in response to cVA. Est-6° mutant males had a lower threshold of behavioral response to cVA, as revealed by the analysis of two cVA-induced behaviors. In particular, mutant males exhibited a strong decrease of male-male courtship, in association with a delay in courtship initiation.

Conclusions

Our study presents evidence that Est-6 plays a role in the physiological and behavioral dynamics of sex pheromone response in Drosophila males and supports a role of Est-6 as an odorant-degrading enzyme (ODE) in male antennae. Our results also expand the role of Est-6 in Drosophila biology, from reproduction to olfaction, and highlight the role of ODEs in insect olfaction.

Keywords:
carboxylesterase; esterase 6; olfaction; pheromone; signal termination